730
Views
113
CrossRef citations to date
0
Altmetric
Review

MF59 adjuvant: the best insurance against influenza strain diversity

, , , &
Pages 447-462 | Published online: 09 Jan 2014

References

  • Vesikari T, Groth N, Karvonen A, Borkowski A, Pellegrini M. MF59-adjuvanted influenza vaccine (FLUAD) in children: safety and immunogenicity following a second year seasonal vaccination. Vaccine27(45), 6291–6295 (2009).
  • Vesikari T, Knuf M, Wutzler P et al. Efficacy of an MF59- Adjuvanted seasonal influenza vaccine versus non-adjuvanted influenza vaccine and control vaccine in 6 to < 72 month old children. Presented at: 48th Annual Meeting of the Infectious Disease Society of America. Vancouver, BC, Canada, 21–24 October 2010.
  • Vesikari T, Pellegrini MF, Karvonen A et al. Enhanced immunogenicity of seasonal influenza vaccines in young children using MF59 adjuvant. Pediatr. Infect. Dis. J.28(7), 563–571 (2009).
  • Goodwin K, Viboud C, Simonsen L. Antibody response to influenza vaccination in the elderly: a quantitative review. Vaccine24(8), 1159–1169 (2006).
  • Bernstein DI, Edwards KM, Dekker CL et al. Effects of adjuvants on the safety and immunogenicity of an avian influenza H5N1 vaccine in adults. J. Infect. Dis.197(5), 667–675 (2008).
  • Galli G, Hancock K, Hoschler K et al. Fast rise of broadly cross-reactive antibodies after boosting long-lived human memory B cells primed by an MF59 adjuvanted prepandemic vaccine. Proc. Natl Acad. Sci. USA106(19), 7962–7967 (2009).
  • Banzhoff A, Gasparini R, Laghi-Pasini F et al. MF59-adjuvanted H5N1 vaccine induces immunologic memory and heterotypic antibody responses in non-elderly and elderly adults. PLoS ONE4(2), e4384 (2009).
  • Fragapane E, Gasparini R, Schioppa F, Laghi-Pasini F, Montomoli E, Banzhoff A. A heterologous MF59-adjuvanted H5N1 prepandemic influenza booster vaccine induces a robust, cross-reactive immune response in adults and the elderly. Clin. Vaccine Immunol.17(11), 1817–1819 (2010).
  • Ott G. The adjuvant MF59: a ten year perspective. In: Vaccine Adjuvants: Preparation Methods and Research Protocols. O’Hagan D (Ed.). Humana Press, New York, NY, USA, 211–228 (2000).
  • Podda A, Del Giudice G. MF59-adjuvanted vaccines: increased immunogenicity with an optimal safety profile. Expert Rev. Vaccines2(2), 197–203 (2003).
  • Schijns V, O’Hagan DT. A safe and potent adjuvant for human use. In: Immunopotentiators in Modern Vaccines, Chapter 9. Podda A, Del Giudice G, O’Hagan DT (Eds). Elsevier Press, Amsterdam, The Netherlands, 149 (2005).
  • O’Hagan DT. MF59 is a safe and potent vaccine adjuvant that enhances protection against influenza virus infection. Expert Rev. Vaccines6(5), 699–710 (2007).
  • Singh M, Ugozzoli M, Kazzaz J et al. A preliminary evaluation of alternative adjuvants to alum using a range of established and new generation vaccine antigens. Vaccine24(10), 1680–1686 (2006).
  • Granoff DM, Mchugh YE, Raff HV, Mokatrin AS, Van Nest G. MF59 adjuvant enhances antibody responses of infant baboons immunized with Haemophilus influenzae type B and Neisseria meningitidis group C oligosaccharide-CRM197 conjugate vaccine. Infect. Immun.65(5), 1710–1715 (1997).
  • Traquina P, Morandi M, Contorni M, Van Nest G. MF59 adjuvant enhances the antibody response to recombinant hepatitis B surface antigen vaccine in primates. J. Infect. Dis.174(6), 1168–1175 (1996).
  • Wack A, Baudner BC, Hilbert AK et al. Combination adjuvants for the induction of potent, long-lasting antibody and T cell responses to influenza vaccine. Vaccine26, 552–561 (2008).
  • Cataldo DM, Van Nest G. The adjuvant MF59 increases the immunogenicity and protective efficacy of subunit influenza vaccine in mice. Vaccine15(16), 1710–1715 (1997).
  • Forrest HL, Khalenkov AM, Govorkova EA, Kim JK, Del Giudice G, Webster RG. Single- and multiple-clade influenza A H5N1 vaccines induce cross protection in ferrets. Vaccine27(31), 4187–4195 (2009).
  • Pellegrini M, Nicolay U, Lindert K, Groth N, Della Cioppa G. MF59-adjuvanted versus non-adjuvanted influenza vaccines: integrated analysis from a large safety database. Vaccine27(49), 6959–6965 (2009).
  • Dupuis M, Mcdonald DM, Ott G. Distribution of adjuvant MF59 and antigen gD2 after intramuscular injection in mice. Vaccine18(5–6), 434–439 (1999).
  • Dupuis M, Murphy TJ, Higgins D et al. Dendritic cells internalize vaccine adjuvant after intramuscular injection. Cell. Immunol.186(1), 18–27 (1998).
  • Seubert A, Monaci E, Pizza M, O’Hagan DT, Wack A. The adjuvants aluminum hydroxide and MF59 induce monocyte and granulocyte chemoattractants and enhance monocyte differentiation toward dendritic cells. J. Immunol.180(8), 5402–5412 (2008).
  • Dupuis M, Denis-Mize K, Labarbara A et al. Immunization with the adjuvant MF59 induces macrophage trafficking and apoptosis. Eur. J. Immunol.31(10), 2910–2918 (2001).
  • Mosca F, Tritto E, Muzzi A et al. Molecular and cellular signatures of human vaccine adjuvants. Proc. Natl Acad. Sci. USA105(30), 10501–10506 (2008).
  • Hui G, Hashimoto C. The requirement of CD80, CD86, and ICAM-1 on the ability of adjuvant formulations to potentiate antibody responses to a Plasmodium falciparum blood-stage vaccine. Vaccine25(51), 8549–8556 (2007).
  • Calabro S, Tortoli M, Baudner BC et al. Vaccine adjuvants alum and MF59 induce rapid recruitment of neutrophils and monocytes that participate in antigen transport to draining lymph nodes. Vaccine29(9), 1812–1823 (2011).
  • Rappuoli R, Del Giudice G. Waiting for a pandemic. In: Infuenza Vaccines for the Future. Rappuoli R, Del Giudice G (Eds). Birkhaeuser, Basel, Switzerland, 261–279 (2008).
  • Carrat F, Flahault A. Influenza vaccine: the challenge of antigenic drift. Vaccine25(39–40), 6852–6862 (2007).
  • De Jong JC, Beyer WE, Palache AM, Rimmelzwaan GF, Osterhaus AD. Mismatch between the 1997/1998 influenza vaccine and the major epidemic A(H3N2) virus strain as the cause of an inadequate vaccine-induced antibody response to this strain in the elderly. J. Med. Virol.61(1), 94–99 (2000).
  • Del Giudice G, Hilbert AK, Bugarini R et al. An MF59-adjuvanted inactivated influenza vaccine containing A/Panama/1999 (H3N2) induced broader serological protection against heterovariant influenza virus strain A/Fujian/2002 than a subunit and a split influenza vaccine. Vaccine24(16), 3063–3065 (2006).
  • Ansaldi F, Bacilieri S, Durando P et al. Cross-protection by MF59-adjuvanted influenza vaccine: neutralizing and haemagglutination-inhibiting antibody activity against A(H3N2) drifted influenza viruses. Vaccine26(12), 1525–1529 (2008).
  • Legrand J, Vergu E, Flahault A. Real-time monitoring of the influenza vaccine field effectiveness. Vaccine24(44–46), 6605–6611 (2006).
  • Du L, Zhou Y, Jiang S. Research and development of universal influenza vaccines. Microbes Infect.12(4), 280–286 (2010).
  • Wiley DC, Wilson IA, Skehel JJ. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature289(5796), 373–378 (1981).
  • Okuno Y, Isegawa Y, Sasao F, Ueda S. A common neutralizing epitope conserved between the hemagglutinins of influenza A virus H1 and H2 strains. J. Virol.67(5), 2552–2558 (1993).
  • Throsby M, Van Den Brink E, Jongeneelen M et al. Heterosubtypic neutralizing monoclonal antibodies cross-protective against H5N1 and H1N1 recovered from human IgM+ memory B cells. PLoS ONE3(12), e3942 (2008).
  • Ekiert DC, Bhabha G, Elsliger MA et al. Antibody recognition of a highly conserved influenza virus epitope. Science324(5924), 246–251 (2009).
  • Sui J, Hwang WC, Perez S et al. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat. Struct. Mol. Biol.16(3), 265–273 (2009).
  • Corti D, Suguitan Al Jr, Pinna D et al. Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal influenza vaccine. J. Clin. Invest.120(5), 1663–1673 (2010).
  • Wang TT, Palese P. Universal epitopes of influenza virus hemagglutinins? Nat. Struct. Mol. Biol.16(3), 233–234 (2009).
  • Schultze V, D’agosto V, Wack A, Novicki D, Zorn J, Hennig R. Safety of MF59 adjuvant. Vaccine26(26), 3209–3222 (2008).
  • Tsai T, Kyaw MH, Novicki D, Nacci P, Rai S, Clemens R. Exposure to MF59-adjuvanted influenza vaccines during pregnancy – a retrospective analysis. Vaccine28(7), 1877–1880 (2010).
  • Black S, Della Cioppa G, Malfroot A et al. Safety of MF59-adjuvanted versus non-adjuvanted influenza vaccines in children and adolescents: an integrated analysis. Vaccine28(45), 7331–7336 (2010).
  • Van Puijenbroek EP, Broos N, Van Grootheest K. Monitoring adverse events of the vaccination campaign against influenza A (H1N1) in The Netherlands. Drug Saf.33(12), 1097–1108 (2010).
  • Banzhoff A, Baxter M, Clemens R, Tsai T. Safety data from clinical trials and pharmacovigilance of mass vaccination with MF59-adjuvated H1N1 influenza vaccines. Safety data from clinical trials and pharmacovigilance of mass vaccination with MF59-adjuvated H1N1 influenza vaccines. Presented at: 28th Annual Meeting of the European Society for Paediatric Infectious Diseases. Nice, France, 4–8 May 2010.
  • Sox H, Fluco C, Liverman T. Gulf War and Health. National Academy Press, Washington, DC, USA, 311 (2000).
  • Phillips CJ, Matyas GR, Hansen CJ, Alving CR, Smith TC, Ryan MA. Antibodies to squalene in US Navy Persian Gulf War veterans with chronic multisymptom illness. Vaccine27(29), 3921–3926 (2009).
  • Del Giudice G, Fragapane E, Bugarini R et al. Vaccines with the MF59 adjuvant do not stimulate antibody responses against squalene. Clin. Vaccine Immunol.13(9), 1010–1013 (2006).
  • Podda A. The adjuvanted influenza vaccines with novel adjuvants: experience with the MF59-adjuvanted vaccine. Vaccine19(17–19), 2673–2680 (2001).
  • Minutello M, Senatore F, Cecchinelli G et al. Safety and immunogenicity of an inactivated subunit influenza virus vaccine combined with MF59 adjuvant emulsion in elderly subjects, immunized for three consecutive influenza seasons. Vaccine17(2), 99–104 (1999).
  • Squarcione S, Sgricia S, Biasio LR, Perinetti E. Comparison of the reactogenicity and immunogenicity of a split and a subunit-adjuvanted influenza vaccine in elderly subjects. Vaccine21(11–12), 1268–1274 (2003).
  • Iorio AM, Francisci D, Camilloni B et al. Antibody responses and HIV-1 viral load in HIV-1-seropositive subjects immunised with either the MF59-adjuvanted influenza vaccine or a conventional non-adjuvanted subunit vaccine during highly active antiretroviral therapy. Vaccine21(25–26), 3629–3637 (2003).
  • Baldo V, Baldovin T, Floreani A, Carraro AM, Trivello R. MF59-adjuvanted influenza vaccine confers superior immunogenicity in adult subjects (18–60 years of age) with chronic diseases who are at risk of post-influenza complications. Vaccine25(20), 3955–3961 (2007).
  • Banzhoff A, Nacci P, Podda A. A new MF59-adjuvanted influenza vaccine enhances the immune response in the elderly with chronic diseases: results from an immunogenicity meta-analysis. Gerontology49(3), 177–184 (2003).
  • Baldo V, Baldovin T, Floreani A, Fragapane E, Trivello R. Response of influenza vaccines against heterovariant influenza virus strains in adults with chronic diseases. J. Clin. Immunol.27(5), 542–547 (2007).
  • Ansaldi F, Bacilieri S, Durando P et al. Humoral response against heterogeneous circulating influenza viruses elicited by MF59- and non-adjuvanted vaccines during seasons with good or partial matching between vaccine strains and isolates. Vaccine28, 4123–4129 (2010).
  • Ansaldi F, Canepa P, Parodi V et al. Adjuvanted seasonal influenza vaccines and perpetual viral metamorphosis: the importance of cross-protection. Vaccine27(25–26), 3345–3348 (2009).
  • Puig-Barbera J, Diez-Domingo J, Perez Hoyos S, Belenguer Varea A, Gonzalez Vidal D. Effectiveness of the MF59-adjuvanted influenza vaccine in preventing emergency admissions for pneumonia in the elderly over 64 years of age. Vaccine23(3), 283–289 (2004).
  • Puig-Barbera J, Diez-Domingo J, Varea AB et al. Effectiveness of MF59-adjuvanted subunit influenza vaccine in preventing hospitalisations for cardiovascular disease, cerebrovascular disease and pneumonia in the elderly. Vaccine25(42), 7313–7321 (2007).
  • Mannino S, Villa M, Weiss N, Apolone G, Rothman K. Effectiveness of influenza vaccination with FLUAD versus a Sub-unit Influenza Vaccine Society for Epidemiologic Research (SER). Effectiveness of influenza vaccination with FLUAD versus a Sub-unit Influenza Vaccine Society for Epidemiologic Research (SER). Am. J. Epidemiol.171(Suppl.), S157 (2010).
  • Monto AS, Whitley RJ. Seasonal and pandemic influenza: a 2007 update on challenges and solutions. Clin. Infect. Dis.46(7), 1024–1031 (2008).
  • Jennings LC, Monto AS, Chan PK, Szucs TD, Nicholson KG. Stockpiling prepandemic influenza vaccines: a new cornerstone of pandemic preparedness plans. Lancet Infect. Dis.8(10), 650–658 (2008).
  • Partridge J, Kieny MP. Global production of seasonal and pandemic (H1N1) influenza vaccines in 2009–2010 and comparison with previous estimates and global action plan targets. Vaccine28(30), 4709–4712 (2010).
  • Ducatez MF, Bahl J, Griffin Y et al. Feasibility of reconstructed ancestral H5N1 influenza viruses for cross-clade protective vaccine development. Proc. Natl Acad. Sci. USA108(1), 349–354 (2011).
  • Leroux-Roels G. Prepandemic H5N1 influenza vaccine adjuvanted with AS03: a review of the pre-clinical and clinical data. Expert Opin. Biol. Ther.9(8), 1057–1071 (2009).
  • Levie K, Leroux-Roels I, Hoppenbrouwers K et al. An adjuvanted, low-dose, pandemic influenza A (H5N1) vaccine candidate is safe, immunogenic, and induces cross-reactive immune responses in healthy adults. J. Infect. Dis.198(5), 642–649 (2008).
  • Alberini I, Del Tordello E, Fasolo A et al. Pseudoparticle neutralization is a reliable assay to measure immunity and cross-reactivity to H5N1 influenza viruses. Vaccine27(43), 5998–6003 (2009).
  • Keitel W, Groth N, Lattanzi M et al. Dose ranging of adjuvant and antigen in a cell culture H5N1 influenza vaccine: safety and immunogenicity of a Phase 1/2 clinical trial. Vaccine28(3), 840–848 (2010).
  • Vesikari T, Karvonen A, Tilman S et al. Immunogenicity and safety of MF59-adjuvanted H5N1 influenza vaccine from infancy to adolescence. Pediatrics126(4), e762–e770 (2010).
  • Stephenson I, Bugarini R, Nicholson KG et al. Cross-reactivity to highly pathogenic avian influenza H5N1 viruses after vaccination with nonadjuvanted and MF59-adjuvanted influenza A/Duck/Singapore/97 (H5N3) vaccine: a potential priming strategy. J. Infect. Dis.191(8), 1210–1215 (2005).
  • Stephenson I, Nicholson KG, Colegate A et al. Boosting immunity to influenza H5N1 with MF59-adjuvanted H5N3 A/Duck/Singapore/97 vaccine in a primed human population. Vaccine21(15), 1687–1693 (2003).
  • Leroux-Roels I, Bernhard R, Gerard P, Drame M, Hanon E, Leroux-Roels G. Broad clade 2 cross-reactive immunity induced by an adjuvanted clade 1 rH5N1 pandemic influenza vaccine. PLoS ONE3(2), e1665 (2008).
  • Chu DW, Hwang SJ, Lim FS et al. Immunogenicity and tolerability of an AS03(A)-adjuvanted prepandemic influenza vaccine: a Phase III study in a large population of Asian adults. Vaccine27(52), 7428–7435 (2009).
  • Baras B, Stittelaar KJ, Simon JH et al. Cross-protection against lethal H5N1 challenge in ferrets with an adjuvanted pandemic influenza vaccine. PLoS ONE3(1), e1401 (2008).
  • Ehrlich HJ, Muller M, Oh HM et al. A clinical trial of a whole-virus H5N1 vaccine derived from cell culture. N. Engl. J. Med.358(24), 2573–2584 (2008).
  • Wu J, Fang HH, Chen JT et al. Immunogenicity, safety, and cross-reactivity of an inactivated, adjuvanted, prototype pandemic influenza (H5N1) vaccine: a Phase II, double-blind, randomized trial. Clin. Infect. Dis.48(8), 1087–1095 (2009).
  • Lopez P, Caicedo Y, Sierra A. Sequential, concurrent and mixed administration of seasonal influenza and MF59®-adjuvanted H5N1 vaccines: a Phase II, randomised, controlled trial of immunogenicity and safety in healthy adults. J. Infect. Dis. (2011) (In Press).
  • Keitel W, Groth N, Lattanzi M, Praus M, Hilbert AK, Tsai TF. Dose ranging of adjuvant and antigen in a cell culture H5N1 influenza vaccine: safety and immunogenicity of a Phase 1/2 clinical trial. Vaccine28(3), 840–848 (2009).
  • Greenberg ME, Lai MH, Hartel GF et al. Response to a monovalent 2009 influenza A (H1N1) vaccine. N. Engl. J. Med.361(25), 2405–2413 (2009).
  • Arguedas A, Soley C, Lindert K. Responses to 2009 H1N1 vaccine in children 3 to 17 years of age. N. Engl. J. Med.362(4), 370–372 (2010).
  • Clark TW, Pareek M, Hoschler K et al. Trial of 2009 influenza A (H1N1) monovalent MF59-adjuvanted vaccine. N. Engl. J. Med.361(25), 2424–2435 (2009).
  • Yasuda Y, Komatsu R, Matsushita K et al. Comparison of half and full doses of an MF59-adjuvanted cell culture-derived A/H1N1v vaccine in Japanese children. Adv. Ther.27(7), 444–457 (2010).
  • De Donato S, Granoff D, Minutello M et al. Safety and immunogenicity of MF59-adjuvanted influenza vaccine in the elderly. Vaccine17(23–24), 3094–3101 (1999).
  • Camilloni B, Neri M, Lepri E, Iorio AM. Cross-reactive antibodies in middle-aged and elderly volunteers after MF59-adjuvanted subunit trivalent influenza vaccine against B viruses of the B/Victoria or B/Yamagata lineages. Vaccine27(31), 4099–4103 (2009).
  • Galli G, Medini D, Borgogni E et al. Adjuvanted H5N1 vaccine induces early CD4+ T cell response that predicts long-term persistence of protective antibody levels. Proc. Natl Acad. Sci. USA106(10), 3877–3882 (2009).
  • Nicholson KG, Colegate AE, Podda A et al. Safety and antigenicity of non-adjuvanted and MF59-adjuvanted influenza A/Duck/Singapore/97 (H5N3) vaccine: a randomised trial of two potential vaccines against H5N1 influenza. Lancet357(9272), 1937–1943 (2001).
  • Stephenson I, Nicholson KG, Hoschler K et al. Antigenically distinct MF59-adjuvanted vaccine to boost immunity to H5N1. N. Engl. J. Med.359(15), 1631–1633 (2008).
  • Fazekas De St Groth S, Webster RG. Disquisitions of original antigenic sin. I. Evidence in man. J. Exp. Med.124(3), 331–345 (1966).
  • Zangwill KM, Treanor JJ, Campbell JD, Noah DL, Ryea J. Evaluation of the safety and immunogenicity of a booster (third) dose of inactivated subvirion H5N1 influenza vaccine in humans. J. Infect. Dis.197(4), 580–583 (2008).
  • Leroux-Roels I, Roman F, Forgus S et al. Priming with AS03 A-adjuvanted H5N1 influenza vaccine improves the kinetics, magnitude and durability of the immune response after a heterologous booster vaccination: an open non-randomised extension of a double-blind randomised primary study. Vaccine28(3), 849–857 (2010).
  • Ehrlich HJ, Muller M, Fritsch S et al. A cell culture (Vero)-derived H5N1 whole-virus vaccine induces cross-reactive memory responses. J. Infect. Dis.200(7), 1113–1118 (2009).
  • Stohr K. Vaccinate before the next pandemic? Nature465(7295), 161 (2010).
  • Khurana S, Chearwae W, Castellino F et al. Vaccines with MF59 adjuvant expand the antibody repertoire to target protective sites of pandemic avian H5N1 influenza virus. Sci. Transl. Med.2(15), 15ra15 (2010).
  • Khurana S, Suguitan AL Jr, Rivera Y et al. Antigenic fingerprinting of H5N1 avian influenza using convalescent sera and monoclonal antibodies reveals potential vaccine and diagnostic targets. PLoS Med.6(4), e1000049 (2009).
  • Del Giudice G, Stittelaar KJ, Van Amerongen G et al. Seasonal influenza vaccine provides priming for A/H1N1 immunization. Sci. Transl. Med.1(12), 12re11 (2009).
  • Laurie KL, Carolan LA, Middleton D, Lowther S, Kelso A, Barr IG. Multiple infections with seasonal influenza A virus induce cross-protective immunity against A(H1N1) pandemic influenza virus in a ferret model. J. Infect. Dis.202(7), 1011–1020 (2010).
  • Kash JC, Qi L, Dugan VG et al. Prior infection with classical swine H1N1 influenza viruses is associated with protective immunity to the 2009 pandemic H1N1 virus. Influenza Other Respi. Viruses4(3), 121–127 (2010).
  • Skountzou I, Koutsonanos DG, Kim JH et al. Immunity to pre-1950 H1N1 influenza viruses confers cross-protection against the pandemic swine-origin 2009 A (H1N1) influenza virus. J. Immunol.185(3), 1642–1649 (2010).
  • Mccullers JA, Van De Velde LA, Allison KJ, Branum KC, Webby RJ, Flynn PM. Recipients of vaccine against the 1976 ‘swine flu’ have enhanced neutralization responses to the 2009 novel H1N1 influenza virus. Clin. Infect. Dis.50(11), 1487–1492 (2010).
  • Ansaldi F, Zancolli M, Durando P et al. Antibody response against heterogeneous circulating influenza virus strains elicited by MF59- and non-adjuvanted vaccines during seasons with good or partial matching between vaccine strain and clinical isolates. Vaccine28(25), 4123–4129 (2010).

Websites

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.